Retrograde release of endocannabinoids inhibits presynaptic GABA release to second-order baroreceptive neurons in NTS
Abstract In prior studies, we found that activation of cannabinoid-1 receptors in the nucleus tractus solitarii (NTS) prolonged baroreflex-induced sympathoinhibition in rats. In many regions of the central nervous system, activation of cannabinoid-1 receptors presynaptically inhibits γ-aminobutyric...
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| creator | Chen, Chao-Yin Bonham, Ann C Dean, Caron Hopp, Francis A Hillard, Cecilia J Seagard, Jeanne L |
| description | Abstract In prior studies, we found that activation of cannabinoid-1 receptors in the nucleus tractus solitarii (NTS) prolonged baroreflex-induced sympathoinhibition in rats. In many regions of the central nervous system, activation of cannabinoid-1 receptors presynaptically inhibits γ-aminobutyric acid (GABA) release, disinhibiting postsynaptic neurons. To determine if cannabinoid-1 receptor-mediated presynaptic inhibition of GABA release occurs in the NTS, we recorded miniature inhibitory postsynaptic currents in anatomically identified second-order baroreceptive NTS neurons in the presence of ionotropic glutamate receptor antagonists and tetrodotoxin. The cannabinoid-1 receptor agonists, WIN 55212-2 (0.3–30 μM) and methanandamide (3 μM) decreased the frequency of miniature inhibitory postsynaptic currents in a concentration-dependent manner, an effect that was blocked by the cannabinoid-1 receptor antagonist, N-(piperidin-1-yl)-5-(4-iodophenyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide (AM 251, 5 μM). Importantly, depolarization of second-order baroreceptive neurons decreased the frequency of miniature inhibitory postsynaptic currents; an effect which was blocked by the cannabinoid-1 receptor antagonist. The data indicate that depolarization of second-order baroreceptive NTS neurons induces endocannabinoid release from the neurons, leading to activation of presynaptic cannabinoid-1 receptors, inhibition of GABA release and subsequent enhanced baroreflex signaling in the NTS. The data suggest that endocannabinoid signaling in the NTS regulates short-term synaptic plasticity and provide a mechanism for endocannabinoid modulation of central baroreflex control. |
| doi_str_mv | 10.1016/j.autneu.2010.06.001 |
| format | Article |
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In many regions of the central nervous system, activation of cannabinoid-1 receptors presynaptically inhibits γ-aminobutyric acid (GABA) release, disinhibiting postsynaptic neurons. To determine if cannabinoid-1 receptor-mediated presynaptic inhibition of GABA release occurs in the NTS, we recorded miniature inhibitory postsynaptic currents in anatomically identified second-order baroreceptive NTS neurons in the presence of ionotropic glutamate receptor antagonists and tetrodotoxin. The cannabinoid-1 receptor agonists, WIN 55212-2 (0.3–30 μM) and methanandamide (3 μM) decreased the frequency of miniature inhibitory postsynaptic currents in a concentration-dependent manner, an effect that was blocked by the cannabinoid-1 receptor antagonist, N-(piperidin-1-yl)-5-(4-iodophenyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide (AM 251, 5 μM). Importantly, depolarization of second-order baroreceptive neurons decreased the frequency of miniature inhibitory postsynaptic currents; an effect which was blocked by the cannabinoid-1 receptor antagonist. The data indicate that depolarization of second-order baroreceptive NTS neurons induces endocannabinoid release from the neurons, leading to activation of presynaptic cannabinoid-1 receptors, inhibition of GABA release and subsequent enhanced baroreflex signaling in the NTS. The data suggest that endocannabinoid signaling in the NTS regulates short-term synaptic plasticity and provide a mechanism for endocannabinoid modulation of central baroreflex control.</description><identifier>ISSN: 1566-0702</identifier><identifier>EISSN: 1872-7484</identifier><identifier>DOI: 10.1016/j.autneu.2010.06.001</identifier><identifier>PMID: 20580326</identifier><language>eng</language><publisher>Amsterdam: Elsevier B.V</publisher><subject>Advanced Basic Science ; Animals ; Baroreflex ; Baroreflex - drug effects ; Baroreflex - physiology ; Biological and medical sciences ; Brainstem ; Cannabinoid Receptor Modulators - metabolism ; Cannabinoid Receptor Modulators - secretion ; Electrophysiology ; Endocannabinoids ; Excitatory Amino Acid Antagonists - pharmacology ; Fundamental and applied biological sciences. Psychology ; gamma-Aminobutyric Acid - metabolism ; gamma-Aminobutyric Acid - secretion ; Inhibitory Postsynaptic Potentials - drug effects ; Inhibitory Postsynaptic Potentials - physiology ; Male ; Medical Education ; Neural Inhibition - drug effects ; Neural Inhibition - physiology ; Neurons - drug effects ; Neurons - metabolism ; Neurons - secretion ; Peripheral nervous system. Autonomic nervous system. Neuromuscular transmission. Ganglionic transmission. Electric organ ; Presynaptic Terminals - drug effects ; Presynaptic Terminals - metabolism ; Presynaptic Terminals - secretion ; Rat ; Rats ; Rats, Sprague-Dawley ; Sodium Channel Blockers - pharmacology ; Solitary Nucleus - cytology ; Solitary Nucleus - drug effects ; Solitary Nucleus - physiology ; Vertebrates: nervous system and sense organs</subject><ispartof>Autonomic neuroscience, 2010-12, Vol.158 (1), p.44-50</ispartof><rights>Elsevier B.V.</rights><rights>2010 Elsevier B.V.</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2010 Elsevier B.V. All rights reserved.</rights><rights>2010 Elsevier B.V. All rights reserved. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c579t-264265748dfe020a7827c1910de645d1bc985eebccd03c48505e598080d8061f3</citedby><cites>FETCH-LOGICAL-c579t-264265748dfe020a7827c1910de645d1bc985eebccd03c48505e598080d8061f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.autneu.2010.06.001$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23431686$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20580326$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Chao-Yin</creatorcontrib><creatorcontrib>Bonham, Ann C</creatorcontrib><creatorcontrib>Dean, Caron</creatorcontrib><creatorcontrib>Hopp, Francis A</creatorcontrib><creatorcontrib>Hillard, Cecilia J</creatorcontrib><creatorcontrib>Seagard, Jeanne L</creatorcontrib><title>Retrograde release of endocannabinoids inhibits presynaptic GABA release to second-order baroreceptive neurons in NTS</title><title>Autonomic neuroscience</title><addtitle>Auton Neurosci</addtitle><description>Abstract In prior studies, we found that activation of cannabinoid-1 receptors in the nucleus tractus solitarii (NTS) prolonged baroreflex-induced sympathoinhibition in rats. In many regions of the central nervous system, activation of cannabinoid-1 receptors presynaptically inhibits γ-aminobutyric acid (GABA) release, disinhibiting postsynaptic neurons. To determine if cannabinoid-1 receptor-mediated presynaptic inhibition of GABA release occurs in the NTS, we recorded miniature inhibitory postsynaptic currents in anatomically identified second-order baroreceptive NTS neurons in the presence of ionotropic glutamate receptor antagonists and tetrodotoxin. The cannabinoid-1 receptor agonists, WIN 55212-2 (0.3–30 μM) and methanandamide (3 μM) decreased the frequency of miniature inhibitory postsynaptic currents in a concentration-dependent manner, an effect that was blocked by the cannabinoid-1 receptor antagonist, N-(piperidin-1-yl)-5-(4-iodophenyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide (AM 251, 5 μM). Importantly, depolarization of second-order baroreceptive neurons decreased the frequency of miniature inhibitory postsynaptic currents; an effect which was blocked by the cannabinoid-1 receptor antagonist. The data indicate that depolarization of second-order baroreceptive NTS neurons induces endocannabinoid release from the neurons, leading to activation of presynaptic cannabinoid-1 receptors, inhibition of GABA release and subsequent enhanced baroreflex signaling in the NTS. The data suggest that endocannabinoid signaling in the NTS regulates short-term synaptic plasticity and provide a mechanism for endocannabinoid modulation of central baroreflex control.</description><subject>Advanced Basic Science</subject><subject>Animals</subject><subject>Baroreflex</subject><subject>Baroreflex - drug effects</subject><subject>Baroreflex - physiology</subject><subject>Biological and medical sciences</subject><subject>Brainstem</subject><subject>Cannabinoid Receptor Modulators - metabolism</subject><subject>Cannabinoid Receptor Modulators - secretion</subject><subject>Electrophysiology</subject><subject>Endocannabinoids</subject><subject>Excitatory Amino Acid Antagonists - pharmacology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>gamma-Aminobutyric Acid - secretion</subject><subject>Inhibitory Postsynaptic Potentials - drug effects</subject><subject>Inhibitory Postsynaptic Potentials - physiology</subject><subject>Male</subject><subject>Medical Education</subject><subject>Neural Inhibition - drug effects</subject><subject>Neural Inhibition - physiology</subject><subject>Neurons - drug effects</subject><subject>Neurons - metabolism</subject><subject>Neurons - secretion</subject><subject>Peripheral nervous system. Autonomic nervous system. Neuromuscular transmission. Ganglionic transmission. Electric organ</subject><subject>Presynaptic Terminals - drug effects</subject><subject>Presynaptic Terminals - metabolism</subject><subject>Presynaptic Terminals - secretion</subject><subject>Rat</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Sodium Channel Blockers - pharmacology</subject><subject>Solitary Nucleus - cytology</subject><subject>Solitary Nucleus - drug effects</subject><subject>Solitary Nucleus - physiology</subject><subject>Vertebrates: nervous system and sense organs</subject><issn>1566-0702</issn><issn>1872-7484</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkstu1DAUhiMEohd4A4SyQawyHDvxJRukaQUFqQKJlrXl2Ceth4w92MlI8_Y4mukU2HRly_7Pfy7fKYo3BBYECP-wWuhp9DgtKOQn4AsA8qw4JVLQSjSyeZ7vjPMKBNCT4iylFQBIaPnL4oQCk1BTflpMP3CM4S5qi2XEAXXCMvQlehuM9l53zgdnU-n8vevcmMpNxLTzejM6U14tL5bHqDGUCU3wtgrRYiw7HUNEg1m5xTIXGoOffcpvtzevihe9HhK-Ppznxc_Pn24vv1TX36--Xi6vK8NEO1aUN5Sz3IztEShoIakwpCVgkTfMks60kiF2xlioTSMZMGStzF1aCZz09Xnxce-7mbo1WoN-jHpQm-jWOu5U0E79--PdvboLW0VbwUXLssH7g0EMvydMo1q7ZHAYtMcwJdWyhkPNKDypFLymrJGcZGWzV5oYUorYH-shoGa0aqX2aNWMVgFXGW0Oe_t3L8egB5ZZ8O4g0MnooY_aG5cedXVTEy7541AwT37rMKpkHHqD1mVeo7LBPVXJ_wZmcN7lnL9wh2kVpugzVUVUogrUzbyG8xaSvICECFH_AZeN2p0</recordid><startdate>20101208</startdate><enddate>20101208</enddate><creator>Chen, Chao-Yin</creator><creator>Bonham, Ann C</creator><creator>Dean, Caron</creator><creator>Hopp, Francis A</creator><creator>Hillard, Cecilia J</creator><creator>Seagard, Jeanne L</creator><general>Elsevier B.V</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>20101208</creationdate><title>Retrograde release of endocannabinoids inhibits presynaptic GABA release to second-order baroreceptive neurons in NTS</title><author>Chen, Chao-Yin ; Bonham, Ann C ; Dean, Caron ; Hopp, Francis A ; Hillard, Cecilia J ; Seagard, Jeanne L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c579t-264265748dfe020a7827c1910de645d1bc985eebccd03c48505e598080d8061f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Advanced Basic Science</topic><topic>Animals</topic><topic>Baroreflex</topic><topic>Baroreflex - drug effects</topic><topic>Baroreflex - physiology</topic><topic>Biological and medical sciences</topic><topic>Brainstem</topic><topic>Cannabinoid Receptor Modulators - metabolism</topic><topic>Cannabinoid Receptor Modulators - secretion</topic><topic>Electrophysiology</topic><topic>Endocannabinoids</topic><topic>Excitatory Amino Acid Antagonists - pharmacology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>gamma-Aminobutyric Acid - metabolism</topic><topic>gamma-Aminobutyric Acid - secretion</topic><topic>Inhibitory Postsynaptic Potentials - drug effects</topic><topic>Inhibitory Postsynaptic Potentials - physiology</topic><topic>Male</topic><topic>Medical Education</topic><topic>Neural Inhibition - drug effects</topic><topic>Neural Inhibition - physiology</topic><topic>Neurons - drug effects</topic><topic>Neurons - metabolism</topic><topic>Neurons - secretion</topic><topic>Peripheral nervous system. Autonomic nervous system. Neuromuscular transmission. Ganglionic transmission. Electric organ</topic><topic>Presynaptic Terminals - drug effects</topic><topic>Presynaptic Terminals - metabolism</topic><topic>Presynaptic Terminals - secretion</topic><topic>Rat</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Sodium Channel Blockers - pharmacology</topic><topic>Solitary Nucleus - cytology</topic><topic>Solitary Nucleus - drug effects</topic><topic>Solitary Nucleus - physiology</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Chao-Yin</creatorcontrib><creatorcontrib>Bonham, Ann C</creatorcontrib><creatorcontrib>Dean, Caron</creatorcontrib><creatorcontrib>Hopp, Francis A</creatorcontrib><creatorcontrib>Hillard, Cecilia J</creatorcontrib><creatorcontrib>Seagard, Jeanne L</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Autonomic neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Chao-Yin</au><au>Bonham, Ann C</au><au>Dean, Caron</au><au>Hopp, Francis A</au><au>Hillard, Cecilia J</au><au>Seagard, Jeanne L</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Retrograde release of endocannabinoids inhibits presynaptic GABA release to second-order baroreceptive neurons in NTS</atitle><jtitle>Autonomic neuroscience</jtitle><addtitle>Auton Neurosci</addtitle><date>2010-12-08</date><risdate>2010</risdate><volume>158</volume><issue>1</issue><spage>44</spage><epage>50</epage><pages>44-50</pages><issn>1566-0702</issn><eissn>1872-7484</eissn><abstract>Abstract In prior studies, we found that activation of cannabinoid-1 receptors in the nucleus tractus solitarii (NTS) prolonged baroreflex-induced sympathoinhibition in rats. In many regions of the central nervous system, activation of cannabinoid-1 receptors presynaptically inhibits γ-aminobutyric acid (GABA) release, disinhibiting postsynaptic neurons. To determine if cannabinoid-1 receptor-mediated presynaptic inhibition of GABA release occurs in the NTS, we recorded miniature inhibitory postsynaptic currents in anatomically identified second-order baroreceptive NTS neurons in the presence of ionotropic glutamate receptor antagonists and tetrodotoxin. The cannabinoid-1 receptor agonists, WIN 55212-2 (0.3–30 μM) and methanandamide (3 μM) decreased the frequency of miniature inhibitory postsynaptic currents in a concentration-dependent manner, an effect that was blocked by the cannabinoid-1 receptor antagonist, N-(piperidin-1-yl)-5-(4-iodophenyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide (AM 251, 5 μM). Importantly, depolarization of second-order baroreceptive neurons decreased the frequency of miniature inhibitory postsynaptic currents; an effect which was blocked by the cannabinoid-1 receptor antagonist. The data indicate that depolarization of second-order baroreceptive NTS neurons induces endocannabinoid release from the neurons, leading to activation of presynaptic cannabinoid-1 receptors, inhibition of GABA release and subsequent enhanced baroreflex signaling in the NTS. The data suggest that endocannabinoid signaling in the NTS regulates short-term synaptic plasticity and provide a mechanism for endocannabinoid modulation of central baroreflex control.</abstract><cop>Amsterdam</cop><pub>Elsevier B.V</pub><pmid>20580326</pmid><doi>10.1016/j.autneu.2010.06.001</doi><tpages>7</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Autonomic neuroscience, 2010-12, Vol.158 (1), p.44-50 |
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| subjects | Advanced Basic Science Animals Baroreflex Baroreflex - drug effects Baroreflex - physiology Biological and medical sciences Brainstem Cannabinoid Receptor Modulators - metabolism Cannabinoid Receptor Modulators - secretion Electrophysiology Endocannabinoids Excitatory Amino Acid Antagonists - pharmacology Fundamental and applied biological sciences. Psychology gamma-Aminobutyric Acid - metabolism gamma-Aminobutyric Acid - secretion Inhibitory Postsynaptic Potentials - drug effects Inhibitory Postsynaptic Potentials - physiology Male Medical Education Neural Inhibition - drug effects Neural Inhibition - physiology Neurons - drug effects Neurons - metabolism Neurons - secretion Peripheral nervous system. Autonomic nervous system. Neuromuscular transmission. Ganglionic transmission. Electric organ Presynaptic Terminals - drug effects Presynaptic Terminals - metabolism Presynaptic Terminals - secretion Rat Rats Rats, Sprague-Dawley Sodium Channel Blockers - pharmacology Solitary Nucleus - cytology Solitary Nucleus - drug effects Solitary Nucleus - physiology Vertebrates: nervous system and sense organs |
| title | Retrograde release of endocannabinoids inhibits presynaptic GABA release to second-order baroreceptive neurons in NTS |
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